Visual Sequences Drive Experience-Dependent Plasticity in Mouse Anterior Cingulate Cortex

Abstract

SUMMARY Mechanisms of experience-dependent plasticity have been well characterized in mouse primary visual cortex (V1), including a form of potentiation driven by repeated presentations of a familiar visual sequence (“sequence plasticity”). The prefrontal anterior cingulate cortex (ACC) responds to visual stimuli, yet little is known about if and how visual experience modifies ACC circuits. We find that mouse ACC exhibits sequence plasticity, but in contrast to V1, the plasticity expresses as a change in response timing, rather than a change in response magnitude. Sequence plasticity is absent in ACC, but not V1, in a mouse model of a neurodevelopmental disorder associated with intellectual disability and autism-like features. Our results demonstrate that simple sensory stimuli can be used to reveal how experience functionally (or dysfunctionally) modifies higher-order prefrontal circuits and suggest a divergence in how ACC and V1 encode familiarity.

The spatiotemporal organization of experience dictates hippocampal involvement in primary visual cortical plasticity

“…Consistent with the idea that hippocampus has a special role in binding relational properties in widely distributed neocortical circuits, recent work has shown that encoding of visual sequences occurs broadly, extending beyond V1 to include anterior cingulate cortex (ACC) (49). We note, however, that although ACC is one of the major intermediaries connecting hippocampus with V1, unlike hippocampus, it is not required for sequence-specific potentiation of VEPs in V1 (49).…”

“…Indeed, anticipatory response modulation within a familiar sequence inherently involves pattern completion (the ability to retrieve a complete record of sensory experience when provided a subset of the original cues), which has been attributed to autoassociative network properties conferred by the anatomical connectivity of the hippocampus (33,47,48). Consistent with the idea that hippocampus has a special role in binding relational properties in widely distributed neocortical circuits, recent work has shown that encoding of visual sequences occurs broadly, extending beyond V1 to include anterior cingulate cortex (ACC) (49). We note, however, that although ACC is one of the major intermediaries connecting hippocampus with V1, unlike hippocampus, it is not required for sequence-specific potentiation of VEPs in V1 (49).…”

The spatiotemporal organization of experience dictates hippocampal involvement in primary visual cortical plasticity

“…In the context of long-loop modulation, an interesting bridge between hippocampus and V1 is the anterior cingulate cortex, [54][55][56] which was recently shown to express sequence-specific VEP potentiation. 57 However, genetic and pharmacogenetic manipulations showed that anterior cingulate cortex is not obligatory for either induction or expression of sequence-specific potentiation in V1. 57 The question remains as to how the hippocampus might be involved in sequence-specific plasticity.…”

“…57 However, genetic and pharmacogenetic manipulations showed that anterior cingulate cortex is not obligatory for either induction or expression of sequence-specific potentiation in V1. 57 The question remains as to how the hippocampus might be involved in sequence-specific plasticity. A clue might be the additional requirement of cholinergic transmission in V1.…”

Expectation violations produce error signals in mouse V1

“…Insights gained from V1 may apply broadly to other regions as well (Douglas & Martin, 2004; Douglas, Martin, & Whitteridge, 1989; Edelman & Mountcastle, 1978; Hawkins & Ahmad, 2016), making this an experimentally accessible area in which to study the cortical basis of predictive processing. In the present study, we investigated predictive processing in the context of a specific form of sequence learning previously described as in V1 (Finnie et al, 2021; Gavornik & Bear, 2014) and anterior cingulate cortex (ACC) (Sidorov et al, 2020). Specifically, we passively exposed mice to rapidly-flashed sequences of sinusoidal gratings, whose spatiotemporal structure differs dramatically from the approximate 1/ f spectrum of their natural environment (Carandini et al, 2005; Ocko, Lindsey, Ganguli, & Deny, 2018; Olshausen & Field, 1997).…”